Unraveling the role of membrane microdomains during microbial infections
Identifieur interne : 000372 ( Pmc/Corpus ); précédent : 000371; suivant : 000373Unraveling the role of membrane microdomains during microbial infections
Auteurs : Prathyusha Bagam ; Dhirendra P. Singh ; Maria Eugenia Inda ; Sanjay BatraSource :
- Cell Biology and Toxicology [ 0742-2091 ] ; 2017.
Abstract
Infectious diseases pose major socioeconomic and health-related threats to millions of people across the globe. Strategies to combat infectious diseases derive from our understanding of the complex interactions between the host and specific bacterial, viral, and fungal pathogens. Lipid rafts are membrane microdomains that play important role in life cycle of microbes. Interaction of microbial pathogens with host membrane rafts influences not only their initial colonization but also their spread and the induction of inflammation. Therefore, intervention strategies aimed at modulating the assembly of membrane rafts and/or regulating raft-directed signaling pathways are attractive approaches for the. management of infectious diseases. The current review discusses the latest advances in terms of techniques used to study the role of membrane microdomains in various pathological conditions and provides updated information regarding the role of membrane rafts during bacterial, viral and fungal infections.
Url:
DOI: 10.1007/s10565-017-9386-9
PubMed: 28275881
PubMed Central: 7088210
Links to Exploration step
PMC:7088210Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Unraveling the role of membrane microdomains during microbial infections</title><author><name sortKey="Bagam, Prathyusha" sort="Bagam, Prathyusha" uniqKey="Bagam P" first="Prathyusha" last="Bagam">Prathyusha Bagam</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0386 0655</institution-id><institution-id institution-id-type="GRID">grid.263880.7</institution-id><institution>Laboratory of Pulmonary Immuno-Toxicology, Department of Environmental Toxicology, Health Research Center,</institution><institution>Southern University and A&M College,</institution></institution-wrap>Baton Rouge, LA 70813 USA</nlm:aff></affiliation></author><author><name sortKey="Singh, Dhirendra P" sort="Singh, Dhirendra P" uniqKey="Singh D" first="Dhirendra P." last="Singh">Dhirendra P. 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Singh</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0386 0655</institution-id><institution-id institution-id-type="GRID">grid.263880.7</institution-id><institution>Laboratory of Pulmonary Immuno-Toxicology, Department of Environmental Toxicology, Health Research Center,</institution><institution>Southern University and A&M College,</institution></institution-wrap>Baton Rouge, LA 70813 USA</nlm:aff></affiliation></author><author><name sortKey="Inda, Maria Eugenia" sort="Inda, Maria Eugenia" uniqKey="Inda M" first="Maria Eugenia" last="Inda">Maria Eugenia Inda</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="GRID">grid.10814.3c</institution-id><institution-id institution-id-type="ISNI">0000 0001 2097 3211</institution-id><institution>Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas,</institution><institution>Universidad Nacional de Rosario and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),</institution></institution-wrap>Suipacha, Rosario, Argentina</nlm:aff></affiliation></author><author><name sortKey="Batra, Sanjay" sort="Batra, Sanjay" uniqKey="Batra S" first="Sanjay" last="Batra">Sanjay Batra</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0386 0655</institution-id><institution-id institution-id-type="GRID">grid.263880.7</institution-id><institution>Laboratory of Pulmonary Immuno-Toxicology, Department of Environmental Toxicology, Health Research Center,</institution><institution>Southern University and A&M College,</institution></institution-wrap>Baton Rouge, LA 70813 USA</nlm:aff></affiliation></author></analytic><series><title level="j">Cell Biology and Toxicology</title><idno type="ISSN">0742-2091</idno><idno type="eISSN">1573-6822</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Infectious diseases pose major socioeconomic and health-related threats to millions of people across the globe. Strategies to combat infectious diseases derive from our understanding of the complex interactions between the host and specific bacterial, viral, and fungal pathogens. Lipid rafts are membrane microdomains that play important role in life cycle of microbes. Interaction of microbial pathogens with host membrane rafts influences not only their initial colonization but also their spread and the induction of inflammation. Therefore, intervention strategies aimed at modulating the assembly of membrane rafts and/or regulating raft-directed signaling pathways are attractive approaches for the. management of infectious diseases. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Cell Biol Toxicol</journal-id><journal-id journal-id-type="iso-abbrev">Cell Biol. Toxicol</journal-id><journal-title-group><journal-title>Cell Biology and Toxicology</journal-title></journal-title-group><issn pub-type="ppub">0742-2091</issn><issn pub-type="epub">1573-6822</issn><publisher><publisher-name>Springer Netherlands</publisher-name><publisher-loc>Dordrecht</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28275881</article-id><article-id pub-id-type="pmc">7088210</article-id><article-id pub-id-type="publisher-id">9386</article-id><article-id pub-id-type="doi">10.1007/s10565-017-9386-9</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Unraveling the role of membrane microdomains during microbial infections</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bagam</surname><given-names>Prathyusha</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Singh</surname><given-names>Dhirendra P.</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Inda</surname><given-names>Maria Eugenia</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Batra</surname><given-names>Sanjay</given-names></name><address><email>sanjay_batra@subr.edu</email></address><xref ref-type="aff" rid="Aff1">1</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0386 0655</institution-id><institution-id institution-id-type="GRID">grid.263880.7</institution-id><institution>Laboratory of Pulmonary Immuno-Toxicology, Department of Environmental Toxicology, Health Research Center,</institution><institution>Southern University and A&M College,</institution></institution-wrap>Baton Rouge, LA 70813 USA</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="GRID">grid.10814.3c</institution-id><institution-id institution-id-type="ISNI">0000 0001 2097 3211</institution-id><institution>Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas,</institution><institution>Universidad Nacional de Rosario and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),</institution></institution-wrap>Suipacha, Rosario, Argentina</aff></contrib-group><pub-date pub-type="epub"><day>9</day><month>3</month><year>2017</year></pub-date><pub-date pub-type="ppub"><year>2017</year></pub-date><volume>33</volume><issue>5</issue><fpage>429</fpage><lpage>455</lpage><history><date date-type="received"><day>11</day><month>11</month><year>2016</year></date><date date-type="accepted"><day>6</day><month>2</month><year>2017</year></date></history><permissions><copyright-statement>© Springer Science+Business Media Dordrecht 2017</copyright-statement><license><license-p>This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Infectious diseases pose major socioeconomic and health-related threats to millions of people across the globe. Strategies to combat infectious diseases derive from our understanding of the complex interactions between the host and specific bacterial, viral, and fungal pathogens. Lipid rafts are membrane microdomains that play important role in life cycle of microbes. Interaction of microbial pathogens with host membrane rafts influences not only their initial colonization but also their spread and the induction of inflammation. Therefore, intervention strategies aimed at modulating the assembly of membrane rafts and/or regulating raft-directed signaling pathways are attractive approaches for the. management of infectious diseases. The current review discusses the latest advances in terms of techniques used to study the role of membrane microdomains in various pathological conditions and provides updated information regarding the role of membrane rafts during bacterial, viral and fungal infections.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Lipid rafts</kwd><kwd>Microdomains</kwd><kwd>Bacteria</kwd><kwd>Virus</kwd><kwd>Fungus</kwd><kwd>Signaling</kwd><kwd>Caveolae</kwd><kwd>Cholesterol</kwd></kwd-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100000066</institution-id><institution>National Institute of Environmental Health Sciences</institution></institution-wrap></funding-source><award-id>7 R15 ES023151 02</award-id></award-group></funding-group><funding-group><award-group><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/100005640</institution-id><institution>Flight Attendant Medical Research Institute</institution></institution-wrap></funding-source><award-id>123253_YCSA_Faculty</award-id></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© Springer Science+Business Media B.V. 2017</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Introduction</title><p id="Par2">The cell, the basic unit of life, is separated from its surroundings by a selectively permeable cell membrane. Receptors and channels within cell membranes mediate interactions between environmental factors and cells. Early concepts of cell membranes envisioned a thin film of lipoidal material coating water-soluble proteins and surrounding the living cell. This model, which allowed for selective membrane permeability, was superseded by the fluid mosaic model of Singer and Nicholson (Singer and Nicolson <xref ref-type="bibr" rid="CR258">1972</xref>). According to the fluid mosaic model, cell membranes are two-dimensional liquid organelles with random distribution of phospholipids and proteins in no specific organization pattern. Since introduction of this concept, there have been revolutionary changes regarding the concept of the plasma membrane and this has been an area of intense research. For example, the existence of detergent-resistant sphingolipid-rich domains was demonstrated by Yu et al. (<xref ref-type="bibr" rid="CR306">1973</xref>) and asymmetric distribution of phospholipids in the plasma membrane of erythrocytes were demonstrated by van Meer and coworkers (van Meer et al. <xref ref-type="bibr" rid="CR285">1980</xref>, <xref ref-type="bibr" rid="CR286">1987</xref>). Further, Simons and Ikonen (<xref ref-type="bibr" rid="CR256">1997</xref>) (Simons and Ikonen <xref ref-type="bibr" rid="CR256">1997</xref>) proposed a glycosphingolipid/cholesterol raft model based on the formation of lateral lipid assemblies in an unsaturated glycerophospholipid environment. Since then, several reports have shown that the plasma membrane is actually more mosaic than fluid (Pike <xref ref-type="bibr" rid="CR219">2003</xref>; Engelman <xref ref-type="bibr" rid="CR67">2005</xref>; Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>), and that the lipids are not randomly distributed. This has lead to the current model in which the plasma membrane is patchy, with segregated portions that are distinct in structure and function and may vary in thickness and composition (Pike <xref ref-type="bibr" rid="CR219">2003</xref>; Garcia-Marcos et al. <xref ref-type="bibr" rid="CR79">2006</xref>; Pike <xref ref-type="bibr" rid="CR221">2009</xref>). The formation of rafts is thought to be mediated by attractive forces between sphingolipids with saturated hydrocarbon chains and cholesterol. This model is based on the fact that formation of lipid rafts cannot be based only on lipid-protein interactions as it also depends on lipid-lipid associations, which includes phase separation coupled with lateral associations. These associations involve formation of hydrogen bonds, electrostatic forces, van der Waals forces, hydrophobic, and hydrophilic interactions (Pike <xref ref-type="bibr" rid="CR221">2009</xref>; Riethmuller et al. <xref ref-type="bibr" rid="CR232">2006</xref>; Nicolson <xref ref-type="bibr" rid="CR192">2014</xref>). In a seminal talk given at the Keystone Symposium on Lipid Rafts and Cell Function (2006) in Steamboat Springs, CO, lipid rafts were defined as small (10–200 nm), heterogeneous, highly dynamic, and sterol- and sphingolipid-rich domains that compartmentalize cellular processes (Pike <xref ref-type="bibr" rid="CR220">2006</xref>). At this Keynote Symposium, it was also suggested that small rafts can sometimes be stabilized to form larger platforms through protein-protein and protein-lipid interactions.</p><p id="Par3">Lipid rafts are enriched in sphingolipids like sphingomyelin and cholesterol and have a preponderance of saturated acyl chains (Mishra and Joshi <xref ref-type="bibr" rid="CR178">2007</xref>; Lingwood and Simons <xref ref-type="bibr" rid="CR152">2010</xref>). Membrane proteins are attached via glycosylphosphatidylinositol (GPI) anchors to the lipid raft entities. The signaling proteins which reside or translocate to the rafts include Ras, nitric oxide synthase (NOS), phosphatidylinositol 3-kinase (PI3K), tyrosine kinases including Fyn and Src, insulin, and epidermal growth factors to name a few. These membrane domains/rafts exert their actions by separating or concentrating specific membrane proteins and lipids within microdomains, which were earlier thought to serve as platforms in the trans-Golgi network for apical membrane sorting and as foci for the recruitment and concentration of signaling molecules at the plasma membrane (Alonso and Millan <xref ref-type="bibr" rid="CR6">2001</xref>). The receptors and stimuli that induce the formation of rafts include cluster of differentiation (CD)5, CD20, CD40, CD95, bacterial and viral infections, as well as exposure to UV light, γ-irradiation, and chemical agents (Bollinger et al. <xref ref-type="bibr" rid="CR31">2005</xref>). Numerous proteins involved in cell signaling have been identified in caveolae and lipid rafts (planar), suggesting that these structures function as signal transduction moieties. Depletion of membrane cholesterol through the use of cholesterol-binding drugs or by blocking cellular cholesterol biosynthesis disrupts the formation and function of both lipid rafts and caveolae, indicating that these membrane domains are involved in a wide range of biological processes. The role of lipid rafts in bringing together specific set of proteins in response to stimulus has been extensively documented in the literature (Simons and Toomre <xref ref-type="bibr" rid="CR257">2000</xref>; Lafont and van der Goot <xref ref-type="bibr" rid="CR138">2005</xref>). Further, lipid rafts can also include or exclude proteins depending on their modifications. For example, palmitoylation increases the affinity of proteins for rafts, but not the ability of proteins to associate with rafts (Melkonian et al. <xref ref-type="bibr" rid="CR175">1999</xref>). Another example is monomeric transmembrane proteins which only reside in rafts for time periods until they are crosslinked or oligomerized (Harder et al. <xref ref-type="bibr" rid="CR107">1998</xref>). The distribution of lipids between the lipid bilayer has also been shown to play an important role in membrane function (Simons and Toomre <xref ref-type="bibr" rid="CR257">2000</xref>).</p><p id="Par4">Caveolins and flotillins constitute a group of proteins that are enriched within lipid rafts (Hansen and Nichols <xref ref-type="bibr" rid="CR106">2009</xref>; Bauer and Pelkmans <xref ref-type="bibr" rid="CR19">2006</xref>; Yao et al. <xref ref-type="bibr" rid="CR302">2009</xref>). Caveolin-1, a palmitoylated membrane protein, is an essential component of a major subclass of rafts known as caveolae (flask-shaped invaginations of the plasma membrane), which causes rafts to polymerize (Rothberg et al. <xref ref-type="bibr" rid="CR236">1992</xref>; Anderson <xref ref-type="bibr" rid="CR9">1998</xref>). In contrast, planar rafts have flotillins as essential components (Giri et al. <xref ref-type="bibr" rid="CR87">2007</xref>; Zhao et al. <xref ref-type="bibr" rid="CR311">2011</xref>). Three caveolin isoforms transcribed from different genes have been identified so far which include caveolin-1, caveolin-2, and caveolin-3. The role of caveolin-1 and caveolin-3 in the formation of caveolae is well documented; however, the role of caveolin-2 is unclear (Sowa et al. <xref ref-type="bibr" rid="CR262">2008</xref>; Drab et al. <xref ref-type="bibr" rid="CR63">2001</xref>; Razani et al. <xref ref-type="bibr" rid="CR230">2001</xref>). Caveolin-1 mediates activation of insulin receptor-β and regulation of the angiotensin/TGF-β pathways suggesting a role in diabetes (Yamamoto et al. <xref ref-type="bibr" rid="CR301">1998</xref>) and pulmonary and cardiac fibrosis, (Wang et al. <xref ref-type="bibr" rid="CR295">2006</xref>; Cohen et al. <xref ref-type="bibr" rid="CR49">2003</xref>), respectively. On the other hand, caveolin-3 defects are associated with muscular dystrophy (autosomal dominant limb girdle muscular dystrophy, idiopathic hyperCKemia, rippling muscle disease, and distal myopathy) (Minetti et al. <xref ref-type="bibr" rid="CR177">1998</xref>; Betz et al. <xref ref-type="bibr" rid="CR25">2001</xref>; Tateyama et al. <xref ref-type="bibr" rid="CR276">2002</xref>). The flotillin family includes flotillin-1 and flotillin-2, which are important for signaling, endocytosis, and interactions of rafts with the cytoskeleton. Functional roles of flotillins have also been documented in polarization and chemotaxis of neutrophils in response to chemo attractants in vivo (Ludwig et al. <xref ref-type="bibr" rid="CR160">2010</xref>; Rossy et al. <xref ref-type="bibr" rid="CR235">2009</xref>). Both types of raft entities are also enriched in cholesterol and glycosphingolipids (Simons and Ikonen <xref ref-type="bibr" rid="CR256">1997</xref>; Korade and Kenworthy <xref ref-type="bibr" rid="CR129">2008</xref>; Wang <xref ref-type="bibr" rid="CR291">2014</xref>). The outer leaflet consists of sphingolipids, phosphatidylcholine, and sphingomyelin, whereas the inner leaflet consists of phosphatidylinositol, phosphatidylethanolamine, and phosphatidylserine with cholesterol being found in both leaflets (Mishra and Joshi <xref ref-type="bibr" rid="CR178">2007</xref>). Enrichment of phospholipids with saturated fatty acids allows close packing of lipids within rafts, and as a result lipid rafts are more complex and less fluid than the surrounding membrane.</p><p id="Par5">Meanwhile, the formation of rafts rich in ceramide following exposure to external stimuli/stress has also received significant attention (Hannun and Obeid <xref ref-type="bibr" rid="CR105">2002</xref>) (Tables <xref rid="Tab1" ref-type="table">1</xref> and <xref rid="Tab2" ref-type="table">2</xref>). Ceramide can be generated by de novo synthesis or hydrolysis of sphingomyelin by sphingomyelinases (Gault et al. <xref ref-type="bibr" rid="CR85">2010</xref>; Silva et al. <xref ref-type="bibr" rid="CR251">2009</xref>). Ceramide is composed of sphingosine and a fatty acid chain, and is found in higher concentrations within the cell membrane. An increasing body of literature has shown ceramide (sphingolipid), as an important molecule that regulates a diverse array of cellular processes including differentiation, immune responses, apoptosis, growth arrest, and senescence (Korade and Kenworthy <xref ref-type="bibr" rid="CR129">2008</xref>; Caliceti et al. <xref ref-type="bibr" rid="CR38">2012</xref>; Arana et al. <xref ref-type="bibr" rid="CR14">2010</xref>; DiNitto et al. <xref ref-type="bibr" rid="CR59">2003</xref>; Castro et al. <xref ref-type="bibr" rid="CR40">2009</xref>; Megha and London <xref ref-type="bibr" rid="CR174">2004</xref>; Yu et al. <xref ref-type="bibr" rid="CR305">2005</xref>). The role of sphingomyelinase and ceramide has been implicated in pathological conditions including pulmonary failure and erythrocyte apoptosis caused by platelet activating factor (Goggel et al. <xref ref-type="bibr" rid="CR88">2004</xref>; Lang et al. <xref ref-type="bibr" rid="CR140">2005</xref>). Furthermore, ceramide is also involved in the fusion of endosomes with lysosomes during the internalization of microbial pathogens into mammalian cells (Bollinger et al. <xref ref-type="bibr" rid="CR31">2005</xref>; Anes et al. <xref ref-type="bibr" rid="CR13">2003</xref>; Gulbins et al. <xref ref-type="bibr" rid="CR99">2004</xref>; Miller et al. <xref ref-type="bibr" rid="CR176">2012</xref>; Hartlova et al. <xref ref-type="bibr" rid="CR108">2010</xref>; Heung et al. <xref ref-type="bibr" rid="CR112">2006</xref>). Conversion of sphingomyelin into ceramide plays an important role in modulation of the membrane structure, which results in membrane vesiculation, fission/fusion and vesicular trafficking and contributes to cellular signaling (Devaux et al. <xref ref-type="bibr" rid="CR56">2008</xref>). Interestingly, rafts on one leaflet of the membrane can induce localized changes in the other leaflet of the bilayer, and they can potentially serve as the link between signals from outside the cell to those produced inside the cell (van Meer et al. <xref ref-type="bibr" rid="CR287">2008</xref>). In addition, ceramide has been shown to form organized, large channels traversing the mitochondrial outer membrane, which leads to the egress of proteins from the intermembrane space. Ceramide may affect the permeability of the mitochondrial outer membrane and the release of cytochrome C (Siskind et al. <xref ref-type="bibr" rid="CR260">2002</xref>). Thus, in the process of apoptosis, the breakdown of plasma membrane sphingomyelin to ceramide results in disorganization of rafts and may regulate apoptotic body formation. High ceramide levels in the lipid rafts increases the size of these platforms due to fusion, and reorganized ceramide-rich rafts retain/restrict proteins differently than other rafts (Spiegel and Milstien <xref ref-type="bibr" rid="CR263">2003</xref>). Ceramide-activated proteins act as secondary messengers and they are directly involved in activation of protein phosphatases PP1 and PP2, isoforms of protein kinase C, cathepsin D, and phospholipase A2, other signaling pathway components, although the precise mechanism of activation is unknown yet. Thus, formation of ceramide may serve different functions at distinct locations in the cell, and therefore, the effects of ceramide rafts are still under investigation (Silva et al. <xref ref-type="bibr" rid="CR251">2009</xref>; Zheng et al. <xref ref-type="bibr" rid="CR312">2006</xref>).<table-wrap id="Tab1"><label>Table 1</label><caption><p>Involvement of ceramide rafts in bacterial infections</p></caption><table frame="hsides" rules="groups"><thead><tr><th>S.No</th><th>Bacteria</th><th>Receptor</th><th>Model used</th><th>Reference</th></tr></thead><tbody><tr><td>1</td><td><italic>Pseudomonas aeruginosa</italic></td><td>CD95 receptor</td><td>(HNEpC)</td><td>(Grassme et al. <xref ref-type="bibr" rid="CR91">2003b</xref>; Grassmé et al. <xref ref-type="bibr" rid="CR94">2001</xref>)</td></tr><tr><td>2</td><td><italic>Neisseria gonorrhea</italic></td><td>CD66 receptor</td><td>Human epithelial cells and primary fibroblasts</td><td>(Hauck et al. <xref ref-type="bibr" rid="CR110">2000</xref>; Grassmé et al. <xref ref-type="bibr" rid="CR92">1997</xref>)</td></tr><tr><td>3</td><td><italic>Staphylococcus aureus</italic></td><td>GPI-anchored proteins</td><td>Human 293 T cells</td><td>(Esen et al. <xref ref-type="bibr" rid="CR69">2001</xref>; Sinha et al. <xref ref-type="bibr" rid="CR259">1999</xref>)</td></tr><tr><td>4</td><td><italic>Mycobacterium avium</italic></td><td>GPI-anchored proteins CR3 and CR4,</td><td>Murine macrophage</td><td>(Maldonado-García et al. <xref ref-type="bibr" rid="CR164">2004</xref>; Irani and Maslow <xref ref-type="bibr" rid="CR121">2005</xref>)</td></tr></tbody></table></table-wrap><table-wrap id="Tab2"><label>Table 2</label><caption><p>Involvement of ceramide rafts in viral infections</p></caption><table frame="hsides" rules="groups"><thead><tr><th>S.No</th><th>Viruses</th><th>Receptor</th><th>Model used</th><th>References</th></tr></thead><tbody><tr><td>1</td><td>Rhinovirus</td><td>ICAM-1</td><td>Hela epithelial cells and WI-38 fibroblasts</td><td>(Greve et al. <xref ref-type="bibr" rid="CR95">1989</xref>; Staunton et al. <xref ref-type="bibr" rid="CR265">1989</xref>; Arruda et al. <xref ref-type="bibr" rid="CR15">1994</xref>)</td></tr><tr><td>2</td><td>Dengue virus</td><td>ICAM, Heat shock proteins (HSP)-HSP90 and 70, Fcγ receptor</td><td>Human myelomonocyte cell line U937</td><td>(Reyes-del Valle et al. <xref ref-type="bibr" rid="CR231">2005</xref>; H Puerta-Guardo et al. <xref ref-type="bibr" rid="CR224">2010</xref>; Takahashi and Suzuki <xref ref-type="bibr" rid="CR274">2011b</xref>)</td></tr><tr><td>3</td><td>Hepatitis C virus (HCV)</td><td>CD81, SR-BI</td><td>Huh-7 cells</td><td>(Kapadia et al. <xref ref-type="bibr" rid="CR125">2007</xref>)</td></tr><tr><td>4</td><td>HIV-1 (human immunodeficiency virus)</td><td>Chemokine receptors-CXCR4/CCR5 and CD4</td><td>CD4+ cells, human embryonic kidney 293 T cells, H9 leukemic T cells and Peripheral blood mononuclear cells (PBMC)</td><td>(Dragic et al. <xref ref-type="bibr" rid="CR64">1996</xref>; Hill and Littman <xref ref-type="bibr" rid="CR113">1996</xref>; Ostrowski et al. <xref ref-type="bibr" rid="CR205">1998</xref>)</td></tr><tr><td>5</td><td>Influenza virus</td><td>Sialic acid and GPI-anchored proteins</td><td>GM 95 cells, mouse B16 melanoma cells</td><td>(Suzuki et al. <xref ref-type="bibr" rid="CR270">2000</xref>; Matrosovich et al. <xref ref-type="bibr" rid="CR170">2006</xref>)</td></tr><tr><td>6</td><td>Ebola virus</td><td>GPI- anchored protein and folate receptor (FRα)</td><td>Human 293 T cells</td><td>(Takahashi and Suzuki <xref ref-type="bibr" rid="CR274">2011b</xref>; Chan et al. <xref ref-type="bibr" rid="CR41">2001</xref>)</td></tr><tr><td>7</td><td>Measles virus</td><td>CD46 and signaling lymphocyte-activation molecule (SLAM)</td><td>T and B cells, CD46-transgenic mice, HeLa cells, and the established murine lung and kidney cultures</td><td>(Dhiman et al. <xref ref-type="bibr" rid="CR57">2004</xref>; Blixenkrone-Møller et al. <xref ref-type="bibr" rid="CR30">1998</xref>)</td></tr></tbody></table></table-wrap></p></sec><sec id="Sec2"><title>Techniques used to study the formation and functions of lipid rafts</title><p id="Par6">Ordered and tightly packed acyl chains in lipid raft domains render them the ability to withstand disruption by non-ionic detergents, whereas the low protein/lipid ratio gives them much lower density than other solubilized membrane proteins. Utilizing this property, lipid rafts were originally isolated by sucrose density gradient ultracentrifugation from cellular extracts prepared in 1% Triton-X (Mishra and Joshi <xref ref-type="bibr" rid="CR178">2007</xref>; Ostrom and Liu <xref ref-type="bibr" rid="CR204">2007</xref>). Several other detergents have subsequently been used to isolate rafts. An alternative approach to study the role of lipid rafts or the association of certain components with rafts is treating them with cholesterol-sequestering agents or chelators like methyl-β-cyclodextrin to disrupt/deplete lipid raft constituents. Moreover, exogenous unsaturated fatty acids, gangliosides or cholesterol can also be used to destabilize raft assembly (Ostrom and Liu <xref ref-type="bibr" rid="CR204">2007</xref>; Brown <xref ref-type="bibr" rid="CR33">2006</xref>). The drawback of using a cholesterol-sequestering agent or chelator is the possible induction of structural or metabolic changes. Therefore, these may not be appropriate options to determine raft-associated cellular changes. Alternatively, genetic approaches such as small interfering RNA (siRNA) or gene knockout animals are widely used to disrupt planar rafts or caveolae (Pelkmans et al. <xref ref-type="bibr" rid="CR214">2004</xref>; Maguy et al. <xref ref-type="bibr" rid="CR163">2006</xref>). These studies address the physiological importance of membrane microdomains and help to determine their importance in signal transduction and bacterial/viral entry into cells (Zhong et al. <xref ref-type="bibr" rid="CR313">2008</xref>).</p><p id="Par7">Recent use of more advanced and non-disruptive techniques have significantly advanced our understanding about these highly dynamic and fragile rafts. These include fluorescence correlation spectroscopy (FCS), single-molecule tracking microscopy (Kusumi et al. <xref ref-type="bibr" rid="CR135">2014</xref>; Parton and del Pozo <xref ref-type="bibr" rid="CR209">2013</xref>; Gambin et al. <xref ref-type="bibr" rid="CR78">2014</xref>), the use of a 2-dimethylamino-6-lauroylnaphthalene (laurdan) labeling probe for studying lateral organization of membranes using conventional confocal microscopy (Dodes Traian et al. <xref ref-type="bibr" rid="CR60">2012</xref>), and fluorescence resonance energy transfer (FRET) for determining the formation and influence of lipid rafts (Silvius and Nabi <xref ref-type="bibr" rid="CR253">2006</xref>). The sensitivity of the FCS technique for the determination of phase separation using free standing artificial lipid bilayers was demonstrated in earlier reports (Korlach et al. <xref ref-type="bibr" rid="CR130">1999</xref>; Bacia et al. <xref ref-type="bibr" rid="CR16">2004</xref>). This technique utilizes excitation and detection as in scanning microscopy to determine temporal fluorescence fluctuations due to the diffusion of individual fluorescent molecules. The autocorrelation curve generated from these fluctuations is used to determine the mobility (diffusion coefficients) of particles and can be used to monitor a single molecule to hundreds of molecules (Schutz et al. <xref ref-type="bibr" rid="CR244">2000</xref>; Ha <xref ref-type="bibr" rid="CR102">2001a</xref>, <xref ref-type="bibr" rid="CR103">b</xref>). Further advancement in fluorescence microscopy techniques came with single molecule imaging (SMI) or single molecule tracking (SMT). This technique provides the ability to monitor collisions, interactions, binding, dissociation, organization, concentration, and disengagement of molecules in living cells with some limitations (Kusumi et al. <xref ref-type="bibr" rid="CR135">2014</xref>; Kusumi et al. <xref ref-type="bibr" rid="CR134">2005a</xref>; <xref ref-type="bibr" rid="CR133">2005b</xref>). Therefore, SMT, which is performed using high resolution photon detector(s) to track only one molecule or to simultaneously image thousands of molecules, has significantly advanced understanding of the three-tiered architecture of plasma membrane (Hinner and Johnsson <xref ref-type="bibr" rid="CR114">2010</xref>). In conjugation with FRET, SMT can also be used to detect activation of single molecules. The combination of these two techniques was first used to assess the activation of the G protein Ras (fluorescently labeled), which functions downstream of receptor-type tyrosine kinases, by detecting its binding the fluorescent GTP (energy acceptor) (Murakoshi et al. <xref ref-type="bibr" rid="CR182">2004</xref>). Moreover, a fluorescent membrane probe, Laurdan, can be used to determine the extent of water penetration into the lipid bilayer enabling assessment of lipid packing and membrane fluidity. The photophysical properties of laurdan determine its spectral sensitivity in polar solvents and leads to a shift of its emission spectra in loosely packed membranes with higher water penetrability (Dodes Traian et al. <xref ref-type="bibr" rid="CR60">2012</xref>; Kwiatek et al. <xref ref-type="bibr" rid="CR136">2013</xref>). The studies conducted using these techniques not only support the existence of rafts in live cells, but electron paramagnetic resonance studies and single molecule tracking methods have been used to determine the half-life of rafts and to assess their interactions with various proteins, respectively (Swamy et al. <xref ref-type="bibr" rid="CR271">2006</xref>). As a result, it is now clear that the half-life of rafts is in the range of 10<sup>2</sup> ns, which is not only faster than the rate of many enzyme reactions, but also less than the half-life of interactions between several proteins known to be involved in signal transduction (Swamy et al. <xref ref-type="bibr" rid="CR271">2006</xref>). Thus, there was imminent need for improving techniques for isolation of membrane rafts and for exploring the functional changes involved in signaling. In this regard, a recent study by Doughty et al. used secondary ion mass spectrometry (Nano SIMS) technology to determine the subcellular localization of hopanoid lipids in bacteria using stable-isotope labeling (Doughty et al. <xref ref-type="bibr" rid="CR62">2014</xref>). The SIMS technique, however, uses primary ions like Cs<sup>+</sup> or O<sup>−</sup> to bombard the surface of sample resulting in generation of secondary ions that are then measured by mass spectrometry. Images are formed from the collection of mass spectra data from several spots on the surface. This technique can also be utilized to determine isotope ratios with high precision and used to visualize labeled sample regions (Altelaar et al. <xref ref-type="bibr" rid="CR7">2006</xref>; Grignon <xref ref-type="bibr" rid="CR96">2007</xref>). Furthermore, advances in microscopy techniques utilizing fluorescent labels or genetically-encoded probes and the mini-singlet–oxygen generator (miniSOG) to visualize the subcellular localization of proteins and lipids by electron microscopy moved the field forward significantly (Huang et al. <xref ref-type="bibr" rid="CR116">2009a</xref>). Additionally, new super-resolution microscopy techniques such as 3D-structured illumination microscopy (SIM), photoactivated localization microscopy (PALM), stochastic optical reconstruction (STORM), and stimulated emission depletion microscopy (STED) allow the investigation of lipid rafts at a level that was previously unattainable (Huang et al. <xref ref-type="bibr" rid="CR116">2009a</xref>). Among these, SIM is an ultra-resolution light microscopy technique that utilizes patterned illumination from a coherent light source to observe structures below the resolution limit of light microscopy by generating difference/beat frequencies termed <italic>Moiré fringes</italic>. This technique can be used with any conventional fluorophore and cell preparation (Kusumi et al. <xref ref-type="bibr" rid="CR134">2005a</xref>, <xref ref-type="bibr" rid="CR133">b</xref>, <xref ref-type="bibr" rid="CR135">2014</xref>). On the other hand, PALM method is based on serial photoactivation or photoswitching and subsequent bleaching of several randomly scattered fluorescent proteins. This method provides a significant edge over the limitations of electron microscopy and conventional fluorescent microscopy to quantify protein aggregates or view cluster sizes that lie below diffraction limits. Utilizing total internal reflection fluorescence geometry (TIRF) in PALM further improves the detection range of fluorescent molecules. In order to investigate lipid rafts, another important technique which can be utilized is STORM imaging. This method involves several imaging cycles where a fraction of fluorophores are optically resolved in the field of view during each cycle, resulting in a highly accurate determination of individual active fluorophores (Rust et al. <xref ref-type="bibr" rid="CR238">2006</xref>). Yet another important technique in lipid rafts research is the STED technique, which uses non-linear fluorophore responses to improve the resolution and acquire images below the diffraction limit (Kusumi et al. <xref ref-type="bibr" rid="CR135">2014</xref>; Eggeling et al. <xref ref-type="bibr" rid="CR66">2013</xref>; Sahl and Moerner <xref ref-type="bibr" rid="CR239">2013</xref>). Both PALM and STORM techniques, on the contrary utilize mathematical modeling to reconstruct the sub-diffraction limit from multiple sets of diffraction-limited images (Rust et al. <xref ref-type="bibr" rid="CR238">2006</xref>; Sengupta et al. <xref ref-type="bibr" rid="CR246">2011</xref>; Hess et al. <xref ref-type="bibr" rid="CR111">2006</xref>). To summarize, the utilization of novel tools has helped generate deeper insight into the functional aspects of lipid rafts, which will help direct future studies and therapeutic intervention strategies targeting lipid rafts and lipid raft-associated proteins.</p></sec><sec id="Sec3"><title>Lipid rafts and bacterial infections</title><p id="Par8">Lipid rafts have been shown to play an important role during bacterial infections. Evidence of the ruffling of membrane lipids and proteins during pathogen engulfment and requirement for cholesterol during pathogen invasion substantiates this claim. Further, the requirement of raft-associated receptors on epithelial cells, including CD55 on the apical membrane and CD44 on the basolateral membrane, has been reported for bacterial entry (Selvarangan et al. <xref ref-type="bibr" rid="CR245">2000</xref>; Peiffer et al. <xref ref-type="bibr" rid="CR212">1998</xref>; Stuart et al. <xref ref-type="bibr" rid="CR268">2002a</xref>; Oliferenko et al. <xref ref-type="bibr" rid="CR199">1999</xref>). Several strains of bacteria invade phagocytes and non-phagocytic cells through the endocytic pathway in order to avoid the host defense mechanism (Simons and Gruenberg <xref ref-type="bibr" rid="CR255">2000</xref>; Steinberg and Grinstein <xref ref-type="bibr" rid="CR266">2008</xref>; Gruenberg and van der Goot <xref ref-type="bibr" rid="CR98">2006</xref>). Pathogens entering the host cells through the endosome-lysosome pathway involving clathrin-coated pits have the ability to avoid fusion or acidification following fusion with lysosomes to prevent degradation. Recent evidence suggests that these endocytic entry mechanisms are directed by the structure of lipid rafts, which are internalized via clathrin-dependent pathways. After endocytosis lipid rafts can form caveosomes and fuse with the Golgi complex or endoplasmic reticulum, or alternatively, form intracellular vesicles and remain within the organelle. The entry of pathogens via lipid rafts promotes intracellular survival and dissemination within the host. Raft-mediated entry of <italic>Escherichia coli</italic> (<italic>E. coli</italic>), <italic>Shigella flexneri</italic>, <italic>Salmonella thyphymurium</italic>, <italic>Mycobacterium</italic> spp., <italic>Chlamydia</italic> spp., <italic>Ehrlichia chaffeensis</italic>, <italic>Anaplasma phagocytophilum</italic>, <italic>Campylobacter jejuni</italic> (Lafont and van der Goot <xref ref-type="bibr" rid="CR138">2005</xref>; Manes et al. <xref ref-type="bibr" rid="CR166">2003a</xref>), <italic>Listeria monocytogenes</italic> (Seveau et al. <xref ref-type="bibr" rid="CR247">2004</xref>), <italic>Mycoplasma fermantas</italic> (Yavlovich et al. <xref ref-type="bibr" rid="CR303">2006</xref>), and <italic>Sphingomonas</italic> spp. (Ammendolia et al. <xref ref-type="bibr" rid="CR8">2004</xref>) have been studied extensively to find out the role of lipid rafts in the pathogenesis of the bacterial infections. In this regard, role of molecular motors kinesin and cytoplasmic dynein has also been investigated in terms of trafficking of pathogens inside cells towards lysosomal degradation. Molecular motors are important in the transport of organelle cargoes along microtubules in the cell. This transport driven by molecular motors, either unidirectional or bidirectional is regulated through their post-translational modifications, interactions with effector molecules or autoinhibition. Movement of early phagosomes along microtubules is bidirectional manner, and of late phagosomes is unidirectional which promotes its fusion with lysosomes (Grover et al. <xref ref-type="bibr" rid="CR97">2016</xref>). In a recent study, Rai et al. demonstrated that the mobility of early and late phagosomes correlates with the appearance of lipid rafts and clustering of dynein motors in phagosome membrane. The geometrical reorganization allows dyneins within cluster generate cooperative force on a single microtubule and results in rapid directed transport of phagosome which probably promotes phagosome and lysosome fusion leading to pathogen degradation. Disruption of clustering of small lipid microdomains by several pathogens can helps in survival of pathogen inside the host by inhibition of phagosome motion and phagosome-lysosome fusion (Rai et al. <xref ref-type="bibr" rid="CR227">2016</xref>). Interestingly, lysosome function can also be regulated by cholesterol. Further, Deng and coworkers demonstrated that cholesterol depletion can also disrupt lysosome membrane permeability (Deng et al. <xref ref-type="bibr" rid="CR55">2009</xref>). In this line of thought, mycobacteria was shown to exploit lipid rafts to enhance their adaptive fitness and protection from intracellular degradation by lysosomal pathways. Mycobacteria induce recruitment of tryptophan aspartate-containing coat protein (TACO), which associates with the phagosomal membrane in a cholesterol-dependent way and prevents its fusion with lysosomes (Gatfield and Pieters <xref ref-type="bibr" rid="CR83">2000a</xref>). A report by Wang and coworkers demonstrate that depletion of lipid rafts by methyl-β-cyclodextrin resulted in reduced survival and virulence of <italic>Porphyromonas gingivalis</italic>, a periodontal pathogen in the host. Interestingly, lipid rafts disruption was shown to promote the colocalization of internalized <italic>P. gingivalis</italic> with lysosome (Wang and Hajishengallis <xref ref-type="bibr" rid="CR292">2008</xref>). While <italic>Chlamydia trachomatis</italic>, a common sexually transmitted pathogen also use lipid rafts to disguise the phagosome as a vesicles which are derived from Golgi apparatus. These phagosomes are transported to Golgi apparatus to capture sphingolipid-rich vesicles to disguise host defense system (Norkin et al. <xref ref-type="bibr" rid="CR196">2001</xref>). These studies clearly indicate an important role of lipid rafts in pathogen survival beyond entry. Therefore, it is important to understand the mechanism(s) of invasion used by pathogens in order to design the successful strategy for regulating disease pathogenesis.</p><sec id="FPar1"><title>Mechanisms of bacterial entry in cells</title><p id="Par9">Caveolae, Clathrin-coated pits and phagocytosis all provide entry pathways to toxins, and fall within the size range of 60-100 nm, respectively (Conner and Schmid <xref ref-type="bibr" rid="CR50">2003</xref>; Rollason et al. <xref ref-type="bibr" rid="CR233">2007</xref>). Of these, clathrin-coated pits are considered raft-free, while the caveolae pathway has been considered to be raft-mediated. Interestingly, Shiga toxin and the protective antibody against anthrax toxin both associate with rafts on the cell surface and are subsequently internalized via clathrin-coated pits (Kurzchalia <xref ref-type="bibr" rid="CR131">2003</xref>; Sandvig and van Deurs <xref ref-type="bibr" rid="CR240">2002a</xref>, <xref ref-type="bibr" rid="CR241">b</xref>). Association of caveolae with <italic>E. coli</italic>-containing phagosomes has been reported during its cellular entry (Jermy <xref ref-type="bibr" rid="CR122">2010</xref>; Zaas et al. <xref ref-type="bibr" rid="CR307">2005</xref>), which reflects that caveolae may provide signaling platforms required for bacterial engulfment.</p></sec><sec id="FPar2"><title>Signaling pathways regulated during bacterial infections</title><p id="Par10">The entry of bacteria through lipid rafts leads to changes in signaling pathways including autophagy, alterations in inflammatory cytokine production, and induction of apoptosis (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). Some bacteria like <italic>Salmonella typhimurium</italic> and <italic>S. flexneri</italic>, modulate host signaling by secreting bacterial invasion effector proteins which associate with membrane rafts (Manes et al. <xref ref-type="bibr" rid="CR165">2003b</xref>; Lafont et al. <xref ref-type="bibr" rid="CR139">2002</xref>; Lacalle et al. <xref ref-type="bibr" rid="CR137">2002</xref>). Further, while cellular entry of certain toxins and bacteria have been found to occur through raft-containing pathways, the step(s) required may differ depending on the pathogens.<fig id="Fig1"><label>Fig. 1</label><caption><p>Role of caveolae and lipid rafts in bacterial entry. Bacteria usually enters the cell through endocytic pathway and survives by avoiding fusion with lysosome. The entry is mediated through caveolae or lipid rafts and can be targeted to a number of different intracellular compartments. Bacteria that enter in a lipid raft-dependent manner trigger signaling pathways including induction of apoptosis and cytokine production</p></caption><graphic xlink:href="10565_2017_9386_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par11">Besides utilizing rafts to generate phagosomes as a survival mechanism within non-professional and professional phagocytic cells (Gatfield and Pieters <xref ref-type="bibr" rid="CR84">2000b</xref>; Kim et al. <xref ref-type="bibr" rid="CR127">2002</xref>; Ferrari et al. <xref ref-type="bibr" rid="CR75">1999</xref>; Watarai et al. <xref ref-type="bibr" rid="CR296">2001</xref>), bacteria like <italic>L. monocytogenes</italic>, an intracellular bacterium, have been shown to augment raft-mediated signaling thereby leading to increased cytokine production at the site of infection (Seveau et al. <xref ref-type="bibr" rid="CR247">2004</xref>; Coconnier et al. <xref ref-type="bibr" rid="CR48">2000</xref>; Parihar et al. <xref ref-type="bibr" rid="CR207">2013</xref>; Gekara et al. <xref ref-type="bibr" rid="CR86">2010</xref>; Barbuddhe and Chakraborty <xref ref-type="bibr" rid="CR18">2008</xref>; Kayal and Charbit <xref ref-type="bibr" rid="CR126">2006</xref>). Moreover, recent studies have shown impaired immune responses and reduced survival of <italic>caveolin-1</italic>-deficient mice in response to pulmonary challenge with <italic>Klebsiella pneumoniae</italic> and <italic>Pseudomonas aeruginosa</italic> (Guo et al. <xref ref-type="bibr" rid="CR100">2012</xref>; Gadjeva et al. <xref ref-type="bibr" rid="CR77">2010</xref>). Further, it was observed that knocking down <italic>caveolin-1</italic> resulted in reduced bacterial clearance and an increase in production of pro-inflammatory cytokines in <italic>Klebsiella</italic>-challenged lung epithelial MLE-12 cells (Guo et al. <xref ref-type="bibr" rid="CR100">2012</xref>). Lipid rafts have thus been proposed to modulate bacterial internalization, which may impact host repair mechanisms, a critical phenomenon for host defense against the possibility of DNA damage caused by <italic>K. pneumoniae</italic> infection (Huang et al. <xref ref-type="bibr" rid="CR119">2013</xref>). It was reported that lungs from <italic>caveolin-1</italic> deficient mice showed suppressed NF-кB activation in response to intraperitoneal injection of lipopolysaccharide, an effect believed to be mediated via endothelial NO synthase (eNOS) (Garrean et al. <xref ref-type="bibr" rid="CR82">2006</xref>) (Fig. <xref rid="Fig2" ref-type="fig">2</xref>). <italic>P. aeruginosa</italic>, on the contrary, induces the formation of ceramide-rich rafts, which not only promote host-pathogen interactions but also induces apoptosis of infected cells (Grassme et al. <xref ref-type="bibr" rid="CR90">2003a</xref>). Together, these studies suggest that lipid rafts play critical roles not only in bacterial entry, but also in influencing the host inflammatory responses critical for promoting or clearing infection.<fig id="Fig2"><label>Fig. 2</label><caption><p>Bacterial entry and interaction with receptor molecules. <bold>a</bold> Entry of bacteria into a host cell involves specific interactions of bacterial PAMPs (e.g., LPS and lipopeptides) with receptor molecules on cell surface, leading to conformational changes in rafts. <bold>b</bold> Upon stimulation by bacterial lipopeptides, TLR2 forms heterodimers with TLR6 in lipid raft domains, while CD14 and CD36 (cluster of differentiation) act as adaptor molecules for ligand transfer onto TLR2/6 heterodimers. Following ligand stimulation TIRAP binds to TLR2 through TIR domains and recruits adaptor protein MyD88, which then activates of TNF receptor associated factor 6 (TRAF6). This pathway induces the activation of NF-кB pathway leading to production and secretion of pro-inflammatory cytokines</p></caption><graphic xlink:href="10565_2017_9386_Fig2_HTML" id="MO2"></graphic></fig></p></sec><sec id="FPar3"><title>Bacterial membrane microdomains</title><p id="Par12">In addition to the role of host cell membrane domains during infections, bacterial proteins appear to recognize specific sites on their own membranes as well. Recently Lopez and Kolter described the existence of functional microdomains in bacterial membranes that harbor homologs of Flotillin-1 (eukaryotic lipid raft protein) and are rich in polyisoprenoids and other signaling and transport proteins (Lopez <xref ref-type="bibr" rid="CR155">2015</xref>; Lopez and Kolter <xref ref-type="bibr" rid="CR156">2010</xref>). Bacterial membrane proteins contained in lipid rafts function similarly to those found in eukaryotes and are involved in cell signaling pathways (Barak and Muchova <xref ref-type="bibr" rid="CR17">2013</xref>). Furthermore, as discussed by Barak and Muchova, differential aspects of a bacterial membrane’s physical characteristics, specifically, a negative curvature (concave) or a positive curvature (convex), are recognized by bacterial proteins. Specifically, membranes with a convex shape are linked with asymmetric cell division. Yet another physical characteristic that is important for the organization/localization of proteins in bacterial membranes is the transmembrane electric potential (Barak and Muchova <xref ref-type="bibr" rid="CR17">2013</xref>). As utilized for study of eukaryotic lipid rafts, the procedure used to analyze bacterial rafts is based on their ability to resist disaggregation by non-ionic detergents followed by separation by sucrose gradient. Studies conducted by Lopez and coworkers demonstrate that the detergent-resistant membranes (DRM) of <italic>S. aureus</italic> involves the proteins required for biofilm formation, virulence, and signaling (Lopez and Kolter <xref ref-type="bibr" rid="CR156">2010</xref>). Moreover, all of these processes can be inhibited by blocking the formation of lipid rafts with the use of small molecules (Bramkamp and Lopez <xref ref-type="bibr" rid="CR32">2015</xref>). Zaragozic acid (ZA), a known inhibitor of squalene synthase, which is involved in the formation of polyisoprenoids , inhibits the formation of lipid rafts resulting in impaired biofilm formation. In a recent study, Somani and coworkers demonstrated constitutive expression of FlotP, a Flotillin-1 homolog in <italic>Bacillus anthracis.</italic> The importance of rafts in the growth, membrane fluidity, and virulence of <italic>B. anthracis</italic> was demonstrated by studies conducted using ZA (Somani et al. <xref ref-type="bibr" rid="CR261">2016</xref>). Evidence of detergent soluble and detergent-resistant membrane fractions in <italic>Bacillus halodurans</italic> and <italic>Bacillus subtilis</italic> and the presence of flotillin-1 like protein (FloT) in the cytoplasmic membrane of the latter was also provided in recent studies (Donovan and Bramkamp <xref ref-type="bibr" rid="CR61">2009</xref>; Zhang et al. <xref ref-type="bibr" rid="CR308">2005</xref>). The membranes microdomains of bacterium <italic>Borrelia burgdorferi</italic>, which causes lime disease, have also been shown to possess properties similar to eukaryotic lipid rafts. Likewise, <italic>B. burgdorferi</italic> domains favor selective incorporation of molecules which are membrane anchored via saturated acyl chains but not those having unsaturated acyl chains (LaRocca et al. <xref ref-type="bibr" rid="CR142">2013</xref>). The other interesting observation reported in this study suggests that any changes in <italic>B. burgdorferi</italic> membrane morphology and integrity may affect the physical connection between flagella and the outer membranes. This may result in loss of flat wave morphology, which changes the membrane permeability leading to loss of flagellar subunits followed by death of spirochetes due to increased sensitivity to secondary osmotic lysis. These events confirm the functional importance of membrane microdomains in <italic>B. burgdorferi</italic> (LaRocca et al. <xref ref-type="bibr" rid="CR142">2013</xref>).</p><p id="Par13">Bacterial membrane microdomains were discovered relatively recently, and therefore, increased understanding is still needed. Future studies need to focus on determining the structural components of bacterial rafts and their biological role in different bacterial species. Further, since the perturbation of bacterial microdomains can affect several physiological processes associated with pathogenesis, this field of study also may open new avenues for the control of bacterial infections.</p></sec></sec><sec id="Sec4"><title>Lipid rafts and viral infections</title><p id="Par14">Viruses are classified into four basic types based on their outer structure. These include the following: enveloped DNA viruses, enveloped RNA viruses, non-enveloped DNA viruses, and non-enveloped RNA viruses. In addition, the general virus cycle of infection is typically divided into four stages: entry, translation, replication, and assembly/release (Fig. <xref rid="Fig3" ref-type="fig">3</xref>). The early stage of viral entry into the host cell involves the binding of the virus to one or more cell-surface receptors followed by entry into the cell (Ono and Freed <xref ref-type="bibr" rid="CR201">2005</xref>). Study of the localization of viral structural proteins and the effects of use of cholesterol/raft disrupting agents on the replication of several viruses have demonstrated the role of membrane microdomains in viral cycle.<fig id="Fig3"><label>Fig. 3</label><caption><p>Entry of virus through lipid rafts. Enveloped viruses enter the cells through direct fusion between the viral membrane and cell-surface receptor or through endocytic-mediated pathway, whereas in non-enveloped viruses are translocated directly into cytoplasm by destruction of the viral capsid. Transcription and replication process of viral genome in non-enveloped viruses takes place in the nucleus but for enveloped viruses it takes place both in nucleus and cytoplasm. After assembly the viral proteins, viral glycoprotein’s and infectious particles of viruses are released from cells via budding process at intracellular membranes (e.g., the ER) and at the plasma membrane which disrupts the humoral and cellular responses of the cell</p></caption><graphic xlink:href="10565_2017_9386_Fig3_HTML" id="MO3"></graphic></fig></p><p id="Par15">Viruses generally enter cells through one of two basic mechanisms: (1) enveloped RNA viruses from the <italic>Rhabdoviridae</italic>, <italic>Flaviviridae</italic>, <italic>Orthomyxoviridae</italic>, and <italic>Togaviridae</italic> families and enveloped DNA viruses from the <italic>Papovaviridae</italic> and <italic>Adenoviridae</italic> families enter through endocytic vesicles and (2) through translocation or penetration of viral particles directly into the cytoplasm, by fusion of the viral envelope at the plasma membrane, or through destruction of the viral capsid as in the case of viruses from the <italic>Paramyxoviridae</italic> family (Takahashi and Suzuki <xref ref-type="bibr" rid="CR273">2011a</xref>). In contrast, viruses from the <italic>Herpesviridae</italic> family utilize both pathways (Takahashi and Suzuki <xref ref-type="bibr" rid="CR273">2011a</xref>). Moreover, most viral genomes of enveloped RNA viruses replicate and are transcribed in the cytosol, while those of enveloped DNA viruses replicate in the nucleus. Progeny viruses subsequently bud and are released from the cell membrane.</p><sec id="FPar4"><title>Involvement of surface receptors in viral entry</title><p id="Par16">There is plethora of information regarding the involvement of cell-surface receptors localized within lipid rafts in facilitating viral entry. In brief, facilitation of HIV-1 entry into the cell by binding to the CD4 receptor causes conformational changes in the surface glycoprotein gp120 resulting in its interaction with CXCR4 or CCR5. These events lead to conformational changes in the transmembrane glycoprotein gp41 leading to unmasking of its fusogenic domain (Fantini et al. <xref ref-type="bibr" rid="CR72">1997</xref>; Hammache et al. <xref ref-type="bibr" rid="CR104">1998</xref>; Hug et al. <xref ref-type="bibr" rid="CR120">2000</xref>). While glycosyl phosphatidylinositol (GPI) anchored folate receptor-α (FRα) localized in membrane rafts is required for the entry of ebola and marburg viruses to enter host cells. The EBV human herpes virus infects B lymphocytes via the human complement receptor type 2 (CR2 aka CD21), which exists as a complex with CD19 and palmitoylated CD81 in lipid rafts. This CD19/21/81 complex functions to prolong the stability of, and signaling via, the B cell antigen receptor (Fingeroth et al. <xref ref-type="bibr" rid="CR76">1984</xref>; Cherukuri et al. <xref ref-type="bibr" rid="CR45">2004</xref>; Birkenbach et al. <xref ref-type="bibr" rid="CR29">1992</xref>). While discussion about all the related studies is beyond the scope of this article, most of the work in this area is referenced in Table <xref rid="Tab3" ref-type="table">3</xref>.<table-wrap id="Tab3"><label>Table 3</label><caption><p>Receptors involved in the entry process of viruses</p></caption><table frame="hsides" rules="groups"><thead><tr><th>S.No</th><th>Family</th><th>Viruses</th><th>Mode of entry</th><th>Receptor</th><th>Model Used</th><th>References</th></tr></thead><tbody><tr><td>1</td><td><italic>Herpesviridae</italic></td><td>Human herpes virus-6 (HHV- 6)</td><td>Membrane rafts</td><td>CD46</td><td>HSB-2 cells</td><td>(Tang et al. <xref ref-type="bibr" rid="CR275">2008</xref>)</td></tr><tr><td>2</td><td><italic>Herpesviridae</italic></td><td>Human herpes virus-8</td><td>Clathrin-dependent pathway</td><td>PI3K,RhoA-GTPase and α3β1 integrins</td><td>HMVEC-d and BCBL-1 cells, HFF cells, 293 cells, HMVEC-d, BJAB, BCBL-1, CHO-B2</td><td>(Raghu et al. <xref ref-type="bibr" rid="CR226">2007</xref>; Akula et al. <xref ref-type="bibr" rid="CR2">2002</xref>; Naranatt et al. <xref ref-type="bibr" rid="CR185">2003</xref>)</td></tr><tr><td>3</td><td><italic>Herpesviridae</italic></td><td>Murine cytomegalovirus (MCMV)</td><td>Clathrin-dependent/caveolae/raft-dependent pathway</td><td>Early endosomal marker EEA-1</td><td>Primary mouse embryonic fibroblasts (MEF), COS-7 and HeLa cells</td><td>(Sharp et al. <xref ref-type="bibr" rid="CR248">2009</xref>; Low et al. <xref ref-type="bibr" rid="CR157">2016</xref>)</td></tr><tr><td>4</td><td><italic>Herpesviridae</italic></td><td>Lymphotrophic herpes virus saimiri (HVS)</td><td>Clathrin-dependent pathway/raft-dependent pathway</td><td>T cell receptor, CD4</td><td>293 T cells, Jurkat T cells</td><td>(Lee et al. <xref ref-type="bibr" rid="CR144">2004</xref>; Cho et al. <xref ref-type="bibr" rid="CR46">2006</xref>)</td></tr><tr><td>5</td><td><italic>Herpesviridae</italic></td><td>Epstein-Bar virus (EBV)</td><td>Endocytic pathway and By Direct fusion with cell-surface membrane</td><td>C3d Complement Receptor (CR2), dynamin, caveolin-1</td><td>B cell lines, B95-8, Mutu I and Mutu III</td><td>(Nemerow et al. <xref ref-type="bibr" rid="CR187">1985</xref>; Nanbo et al. <xref ref-type="bibr" rid="CR184">2013</xref>)</td></tr><tr><td>7</td><td><italic>Herpesviridae</italic></td><td>Herpes simplex virus</td><td>Endocytosis</td><td>Nectin1, heparan sulfate</td><td>HCjE cells</td><td>(Akhtar et al. <xref ref-type="bibr" rid="CR1">2008</xref>; Shukla and Spear <xref ref-type="bibr" rid="CR249">2001</xref>)</td></tr><tr><td>8</td><td><italic>Poxviridae</italic></td><td>Vaccinia virus</td><td>Cholesterol-mediated raft entry</td><td>GM1</td><td>BSC-40 cells</td><td>(Chung et al. <xref ref-type="bibr" rid="CR47">2005</xref>)</td></tr><tr><td>9</td><td><italic>Hepadnaviridae</italic></td><td>Hepatitis B virus</td><td>Clathrin-dependent endocytosis</td><td>Sodium/bile acid co transporting Peptide(SLC10A1)</td><td>HuS-E/2 cells</td><td>(Xiao et al. <xref ref-type="bibr" rid="CR299">2013</xref>; Huang et al. <xref ref-type="bibr" rid="CR117">2012</xref>)</td></tr><tr><td>10</td><td><italic>Adenoviridae</italic></td><td>Simian virus 40</td><td>Clathrin and caveolae-dependent and independent pathway</td><td>MHC class I and ganglioside GM1</td><td>HuH7, African green monkey kidney fibroblasts, CV-1 cells</td><td>(Norkin et al. <xref ref-type="bibr" rid="CR195">2002b</xref>; Damm et al. <xref ref-type="bibr" rid="CR52">2005</xref>; Tsai et al. <xref ref-type="bibr" rid="CR282">2003b</xref>; Anderson et al. <xref ref-type="bibr" rid="CR11">1998b</xref>)</td></tr><tr><td>11</td><td><italic>Papovaviridae</italic></td><td>Bovine papillomavirus</td><td>Clathrin-dependent endocytosis and caveolae-dependent pathway</td><td>Glycosaminoglycan</td><td>293 cells</td><td>(Laniosz et al. <xref ref-type="bibr" rid="CR141">2008</xref>)</td></tr><tr><td>12</td><td><italic>Papovaviridae</italic></td><td>Human papillomavirus</td><td>Clathrin-dependent endocytosis and caveolae-independent pathway</td><td>alpha(6) integrin, heparansulphate proteoglycans and α6 integrin</td><td>HaCaT (epithelium), HeLa (cervix), C33A (cervix), Caski (cervix), T98G (glioblastoma), SK-N-SH (neuroblastoma), OVCAR-4 (ovary), K562 (leukemia), and T47D (breast), and one monkey kidney cell line Cos-7</td><td>(Androutsopoulos et al. <xref ref-type="bibr" rid="CR12">2015</xref>; Yoon et al. <xref ref-type="bibr" rid="CR304">2001</xref>)</td></tr><tr><td>14</td><td><italic>Retroviridae</italic></td><td>Human T lymphotropic virus 1 (HTLV-1)</td><td>Membrane rafts and utilizes Glucose transporter (Glut 1)</td><td>Chemokine receptors-CXCR4/CCR5 and CD4</td><td>K562,MT2 Cell lines, COS, and HEK 293 T cells</td><td>(Pique et al. <xref ref-type="bibr" rid="CR222">1993</xref>; Jones et al. <xref ref-type="bibr" rid="CR123">2006</xref>)</td></tr><tr><td>15</td><td><italic>Retroviridae</italic></td><td>Human immunodeficiency virus (HIV)</td><td>Caveolin-dependent raft and endocytosis pathway</td><td>Chemokine receptors-CXCR4/CCR5 and GPI-anchored proteins, CD4</td><td>Human embryonic kidney 293 T cells, H9 leukemic T cells and peripheral blood mononuclear cells (PBMC), T cell lymphoma cell line, Jurakat, HeLa cells</td><td>(Liao et al. <xref ref-type="bibr" rid="CR150">2001b</xref>; Nguyen and Hildreth <xref ref-type="bibr" rid="CR189">2000</xref>; Nguyen and Taub <xref ref-type="bibr" rid="CR191">2002b</xref>; Alfsen et al. <xref ref-type="bibr" rid="CR3">2005</xref>; Leung et al. <xref ref-type="bibr" rid="CR147">2008b</xref>; Popik et al. <xref ref-type="bibr" rid="CR223">2002</xref>)</td></tr><tr><td>16</td><td><italic>Rhabdoviridae</italic></td><td>Vesicular stomatitis virus (VSV)</td><td>Endocytic pathway/lipid-raft-mediated entry</td><td>GPI-anchored proteins</td><td>Hela cells</td><td>(Patel et al. <xref ref-type="bibr" rid="CR211">2009</xref>)</td></tr><tr><td>17</td><td><italic>Filoviridae</italic></td><td>Ebola virus</td><td>Clathrin-dependent and caveolae-dependent endocytosis</td><td>GPI- anchored protein</td><td>Human 293 T cells</td><td>(Bavari et al. <xref ref-type="bibr" rid="CR21">2002b</xref>)</td></tr><tr><td>18</td><td><italic>Filoviridae</italic></td><td>Japanese encephalitis virus (JEV)</td><td>Clathrin-dependent and caveolae-dependent endocytosis</td><td>GPI-anchored protein- Src/PI3K and lipid raft- mediated entry</td><td>Mouse neural stem cell line C17.2, Huh7, BHK-21, and African green monkey kidney Vero E6 cells, astrocyte cell culture</td><td>(Das et al. <xref ref-type="bibr" rid="CR54">2010b</xref>; Chen et al. <xref ref-type="bibr" rid="CR43">2011a</xref>; Zhu et al. <xref ref-type="bibr" rid="CR314">2012</xref>)</td></tr><tr><td>19</td><td><italic>Filoviridae</italic></td><td>Dengue virus (DEN)</td><td>Lipid-raft-mediated entry</td><td>ICAM, heat shock proteins (HSP)-HSP90 and 70, GPI-anchored proteins</td><td>Human myelomonocyte cell line U937 and association of dengue virus NS1 protein with lipid rafts</td><td>(Reyes-del Valle et al. <xref ref-type="bibr" rid="CR231">2005</xref>; Noisakran et al. <xref ref-type="bibr" rid="CR193">2008</xref>)</td></tr><tr><td>20</td><td><italic>Paramyxoviridae</italic></td><td>Respiratory syncytial virus (RSV)</td><td>Caveolin-mediated endocytosis</td><td>GPI-anchored proteins</td><td>Hep 2 cells and vero C 1008 cells</td><td>(McDonald et al. <xref ref-type="bibr" rid="CR173">2004</xref>; Brown et al. <xref ref-type="bibr" rid="CR36">2002c</xref>)</td></tr><tr><td>21</td><td><italic>Arenaviridae</italic></td><td>Lymphocytic choriomeningitis virus (LCMV)</td><td>Clathrin/caveolin-raft-dependent pathway</td><td>GPI-anchored proteins</td><td>HeLa cells and vero cells</td><td>(Quirin et al. <xref ref-type="bibr" rid="CR225">2008</xref>)</td></tr><tr><td>22</td><td><italic>Coronaviridae</italic></td><td>SARS-CoV, corona virus</td><td>Clathrin-independent and caveolae-independent pathway</td><td>ACE 2 receptor</td><td>Vero E6 cells and HEK 293 T cells</td><td>(Li et al. <xref ref-type="bibr" rid="CR148">2007</xref>; Wang et al. <xref ref-type="bibr" rid="CR294">2008</xref>)</td></tr><tr><td>23</td><td><italic>Flaviviridae</italic></td><td>Human hepatitis C virus (HCV)</td><td>Endocytosis</td><td>CD81 receptor</td><td>Huh-7 cells, HOS. CDR5 cells, Hela and 293 T cell line</td><td>(Zhang et al. <xref ref-type="bibr" rid="CR310">2004</xref>)</td></tr><tr><td>24</td><td><italic>Orthomyxoviridae</italic></td><td>Influenza virus</td><td>Clathrin-independent endocytosis, caveolae-independent endocytosis</td><td>GPI-anchored proteins</td><td>HeLa-T4 cells, MDCK cells (Madin-Darby canine kidney)</td><td>(Cheong et al. <xref ref-type="bibr" rid="CR44">1999</xref>; Zhang et al. <xref ref-type="bibr" rid="CR309">2000</xref>)</td></tr><tr><td>25</td><td><italic>Orthomyxoviridae</italic></td><td>Measles virus</td><td>Raft-mediated</td><td>GPI-anchored proteins, Receptors of H protein- Complement regulatory molecule CD46</td><td>Human B–lymphoblastoid cell line</td><td>(Manié et al. <xref ref-type="bibr" rid="CR167">2000</xref>)</td></tr><tr><td>26</td><td><italic>Togaviridae</italic></td><td>Sindbis virus</td><td>Cholesterol-mediated pathway</td><td>GPI-anchored proteins</td><td>BHK-21 cells</td><td>(Ng et al. <xref ref-type="bibr" rid="CR188">2008</xref>)</td></tr><tr><td>27</td><td><italic>Togaviridae</italic></td><td>Semliki forest virus</td><td>Cholesterol-mediated pathway</td><td>GPI-anchored proteins</td><td>BHK-21 cells</td><td>(Lu and Kielian <xref ref-type="bibr" rid="CR158">2000</xref>)</td></tr><tr><td>28</td><td><italic>Rhabdoviridae</italic></td><td>Rabies virus</td><td>Endocytosis</td><td>GPI-anchored proteins</td><td>BHK-cells</td><td>(Whitt et al. <xref ref-type="bibr" rid="CR297">1991</xref>)</td></tr><tr><td>29</td><td><italic>Picornaviridae</italic></td><td>Echo virus 1</td><td>Caveolae-dependent and membrane raft-dependent endocytosis</td><td>α2β1 integrins and DAF receptors(CD55)</td><td>Green monkey kidney cell line</td><td>(Xing et al. <xref ref-type="bibr" rid="CR300">2004</xref>)</td></tr><tr><td>31</td><td><italic>Picornaviridae</italic></td><td>Enterovirus</td><td>Caveolae-dependent and membraneraft-dependent endocytosis</td><td>DAF receptors</td><td>HT29 cells</td><td>(Stuart et al. <xref ref-type="bibr" rid="CR267">2002b</xref>)</td></tr><tr><td>32</td><td><italic>Picornaviridae</italic></td><td>Rhino virus</td><td>Lipid rafts</td><td>ICAM-1</td><td>Human bronchial epithelial cells and HeLa cells</td><td>(Bentley et al. <xref ref-type="bibr" rid="CR24">2007b</xref>)</td></tr><tr><td>33</td><td><italic>Picornaviridae</italic></td><td>Coxsackie virus</td><td>Clathrin-independent; caveolae/raft-dependent endocytic pathway</td><td>DAF (decay accelerating factor) CD55, MHC class I, and integrins family</td><td>Hela cells, and GMK cells</td><td>(Triantafilou et al. <xref ref-type="bibr" rid="CR280">2002</xref>; Triantafilou and Triantafilou <xref ref-type="bibr" rid="CR278">2003</xref>)</td></tr><tr><td>34</td><td><italic>Picornaviridae</italic></td><td>Rotavirus</td><td>Endocytosis pathway</td><td>Integrins, α2β1 αvβ3 and hsc70 dynamin</td><td>MA104 cells</td><td>(Gutiérrez et al. <xref ref-type="bibr" rid="CR101">2010</xref>)</td></tr><tr><td>35</td><td><italic>Picornaviridae</italic></td><td>Poliovirus</td><td>Receptor-mediated endocytosis</td><td>Poliovirus receptor (CD155)</td><td>African green monkey kidney cells</td><td>(Ohka et al. <xref ref-type="bibr" rid="CR197">2004</xref>)</td></tr><tr><td>36</td><td><italic>Reoviridae</italic></td><td>Blue tongue virus</td><td>Clathrin-dependent and lipid raft-mediated</td><td>SNARE receptor-VP5 (soluble N-ethylmaleimide-sensitive fusion attachment protein receptor)</td><td>BHK cells (baby hamster kidney cell line)and HeLa cells</td><td>(Bhattacharya and Roy <xref ref-type="bibr" rid="CR27">2008b</xref>)</td></tr></tbody></table></table-wrap></p></sec><sec id="FPar5"><title>Mechanisms of viral entry in cells</title><p id="Par17">Following the attachment of non-enveloped viruses to cell-surface receptors, the bound virions can be internalized through a process mediated by rafts involving membrane invaginations and intracytoplasmic vesiculation (Ono and Freed <xref ref-type="bibr" rid="CR201">2005</xref>; Takahashi and Suzuki <xref ref-type="bibr" rid="CR273">2011a</xref>; Suzuki and Suzuki <xref ref-type="bibr" rid="CR269">2006</xref>). This type of viral entry, also termed atypical endocytosis, has been observed for the SV40 (<italic>Papovaviridae</italic> family) virus. Entry of SV40 into target cells is mediated through an association of major histocompatibility complex-1 (MHC-1) with caveolae (Stang et al. <xref ref-type="bibr" rid="CR264">1997</xref>; Anderson et al. <xref ref-type="bibr" rid="CR10">1998a</xref>; Norkin et al. <xref ref-type="bibr" rid="CR194">2002a</xref>; Pelkmans et al. <xref ref-type="bibr" rid="CR215">2001</xref>) or the GM1 ganglioside receptor in lipid rafts (Tsai et al. <xref ref-type="bibr" rid="CR281">2003a</xref>; Pelkmans <xref ref-type="bibr" rid="CR213">2005</xref>). Virus-incorporated caveolae then undergo budding, and the caveolae carries the virus to the endoplasmic reticulum (ER) along cellular microtubules.</p><p id="Par18">Non-enveloped DNA viruses also enter into cells through typical endocytosis utilizing clathrin-dependent or clathrin-independent and caveolae/raft-dependent pathways followed by release of their viral DNA genomes into the cytoplasm by viral capsid destruction (Ono <xref ref-type="bibr" rid="CR200">2010</xref>). Reports suggest that <italic>Coxsackievirus</italic>, which causes aseptic meningitis with symptoms resembling a respiratory disease in addition to flaccid paralysis and chronic myocarditis, utilizes the cellular coxsackievirus and adenovirus receptor for its entry via membrane rafts (Triantafilou and Triantafilou <xref ref-type="bibr" rid="CR278">2003</xref>; <xref ref-type="bibr" rid="CR279">2004</xref>). In addition, several enteroviruses, which cause nerve paralysis, cerebral meningitis, anathema and respiratory symptoms, also utilize caveolae-dependent or raft-dependent endocytosis mechanisms for cellular entry (Stuart et al. <xref ref-type="bibr" rid="CR268">2002a</xref>; Marjomaki et al. <xref ref-type="bibr" rid="CR168">2002</xref>; Upla et al. <xref ref-type="bibr" rid="CR284">2004</xref>; Pietiainen et al. <xref ref-type="bibr" rid="CR218">2005</xref>). In contrast, entry of rhinovirus is mediated by ceramide-rich rafts (Grassme et al. <xref ref-type="bibr" rid="CR93">2005</xref>).</p><p id="Par19">Enveloped viruses also use rafts during the internalization and fusion process. The entry of enveloped viruses involves virus attachment followed by close apposition of the virus and plasma membranes. The two membranes then fuse to deliver the virus’ genomic RNA into the host cells, which requires conversion of the virus-encoded envelope glycoprotein (Env) from its native state to its fusion-activated form (Manes et al. <xref ref-type="bibr" rid="CR166">2003a</xref>; Fantini et al. <xref ref-type="bibr" rid="CR71">2002</xref>; Chazal and Gerlier <xref ref-type="bibr" rid="CR42">2003</xref>; Brown et al. <xref ref-type="bibr" rid="CR35">2002a</xref>)</p></sec><sec id="FPar6"><title>Virus assembly</title><p id="Par20">The later stages of the virus infection cycle involve the assembly of viral components into virions and maturation into infectious particles. Viruses use lipid rafts as a platform because their structure offers an efficient system for concentrating all the viral proteins and glycoproteins required for the assembly of new virions (Ono and Freed <xref ref-type="bibr" rid="CR201">2005</xref>; Suzuki and Suzuki <xref ref-type="bibr" rid="CR269">2006</xref>; Das et al. <xref ref-type="bibr" rid="CR53">2010a</xref>). There is abundant evidence to support the idea that membrane lipids are not randomly incorporated into the viral envelope. Further, it has also been suggested that viral glycoproteins determine the site of virus assembly and budding (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Garoff and Simons <xref ref-type="bibr" rid="CR80">1974</xref>; Garoff et al. <xref ref-type="bibr" rid="CR81">1974</xref>; Allison et al. <xref ref-type="bibr" rid="CR4">1995</xref>; Vennema et al. <xref ref-type="bibr" rid="CR289">1996</xref>; Bruss <xref ref-type="bibr" rid="CR37">2004</xref>). Moreover, in polarized epithelial cells, the viral glycoproteins contain sorting signals or motifs and are directed to the specific site where assembly and budding will occur (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Nayak et al. <xref ref-type="bibr" rid="CR186">2004</xref>). Finally, the lipid composition of the influenza virus family is affected by the affinity of the haemagglutinin and neuraminidase glycoproteins for these lipids, while some reports also suggest that the influenza virus buds from raft domains (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Chazal and Gerlier <xref ref-type="bibr" rid="CR42">2003</xref>; Nayak et al. <xref ref-type="bibr" rid="CR186">2004</xref>). HIV-1 is also enclosed in a lipid envelope enriched in cholesterol and sphingolipids, suggesting specific membrane localization is required for assembly (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Aloia et al. <xref ref-type="bibr" rid="CR5">1993</xref>; Campbell et al. <xref ref-type="bibr" rid="CR39">2001</xref>; Raulin <xref ref-type="bibr" rid="CR229">2002</xref>). With similar methods of assembly and budding within membrane rafts, many other viruses, including influenza virus, measles virus, Ebola virus, and possibly Sendai virus, also use lipid rafts as assembly platforms (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Luo et al. <xref ref-type="bibr" rid="CR161">2008</xref>). In this regard, it was also suggested that the RSV (respiratory syncytial virus) assembles within lipid rafts where viral proteins colocalize with caveolin-1 (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Brown et al. <xref ref-type="bibr" rid="CR35">2002a</xref>, <xref ref-type="bibr" rid="CR34">b</xref>). Taken together, these structures then have the ability to regulate budding; however, the mechanism by which the lipid raft can favor the budding and/or fission process has yet to be explored in detail (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Nayak et al. <xref ref-type="bibr" rid="CR186">2004</xref>; Luo et al. <xref ref-type="bibr" rid="CR161">2008</xref>).</p><p id="Par21">For enveloped viruses, the infectious particles are released from the cell via the budding process. Furthermore, the budding of new virions from the raft allows the exclusion or inclusion of specific host cell membrane proteins in the virus particle, which can disrupt cellular and/or humoral immune responses to the virus (Suzuki and Suzuki <xref ref-type="bibr" rid="CR269">2006</xref>; Das et al. <xref ref-type="bibr" rid="CR53">2010a</xref>). Non-enveloped viruses are released from the infected cell by disrupting the plasma membrane, whereas enveloped viruses contain a host cell-derived lipid bilayer, which is acquired during budding. Only cytolytic viruses lead to disruption of cell integrity, while other viruses are released in a non-destructive manner. In this context, studies demonstrated that ebola and marburg viruses use viral glycoprotein-bearing rafts for budding from host cells. Specifically, VP40 (ebola virus matrix protein) oligomerizes with rafts and plays an important role in assembly and budding(Bavari et al. <xref ref-type="bibr" rid="CR20">2002a</xref>), while glycoprotein complexes composed of gp120 and gp41 along with membrane rafts are used for HIV-1 assembly (Bhattacharya et al. <xref ref-type="bibr" rid="CR28">2004</xref>; Ono et al. <xref ref-type="bibr" rid="CR203">2005</xref>; Ono et al. <xref ref-type="bibr" rid="CR202">2007</xref>; Leung et al. <xref ref-type="bibr" rid="CR146">2008a</xref>). Koshizuka’s group demonstrated the association of HSV-1 UL11 (protein involved in virion maturation) with lipid rafts (Koshizuka et al. <xref ref-type="bibr" rid="CR132">2007</xref>). Among non-enveloped viruses, the association of viral protein VP4 and NSP4-purified virions with lipid rafts have been studied for rotavirus (Sapin et al. <xref ref-type="bibr" rid="CR242">2002</xref>; Cuadras and Greenberg <xref ref-type="bibr" rid="CR51">2003</xref>) while an outer capsid protein important for virus assembly, VP5, was observed to co-purify with lipid raft entities during bluetongue virus infection. The association of VP5 with rafts was shown to depend on membrane docking domain similar to what occurs with the soluble N-ethylmaleimide-sensitive fusion attachment protein receptor (SNARE) family (Bhattacharya and Roy <xref ref-type="bibr" rid="CR26">2008a</xref>). Although rafts are involved in virus assembly, we have to keep in mind that only a fraction of viral proteins are found associated with rafts. However, this could be due to the poor biochemical characterization of raft subsets or to the transient nature of the association (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>).</p></sec><sec id="FPar7"><title>Signaling pathways regulated during viral infections</title><p id="Par22">Since membrane rafts are involved in the entry, assembly, and budding processes of several viruses, it is not surprising that cellular signaling pathways are also affected during viral infections. Lee et al. reported the anti-apoptotic role of PI3K signaling in response to dengue and japanese encephalitis virus (JEV) infections in human lung carcinoma and murine neuroblastoma cell lines (Lee et al. <xref ref-type="bibr" rid="CR145">2005</xref>). However, using microglial cells, Chen and coworkers demonstrated the induction of the Src/Ras±/Raf/ERK/NF-кB pathways leading to induction of TNF-α and IL-1β in response to challenge with JEV (Chen et al. <xref ref-type="bibr" rid="CR43">2011</xref>). This is important because Src-mediated signaling induced by JEV is known to play a critical role in neuronal cell death. Earlier studies revealed the role of lipid rafts in the activation of Src, Ras, Raf, ERK, and NF-кB, which all contribute to JEV-induced TNF-α and IL-1β production (McCubrey et al. <xref ref-type="bibr" rid="CR172">2007</xref>; Wu et al. <xref ref-type="bibr" rid="CR298">2015</xref>). Furthermore, involvement of lipid rafts in Src-mediated signaling pathways upstream of the activation of Raf/ERK/NF-кB has been reported in response to several stimuli (Roux and Blenis <xref ref-type="bibr" rid="CR237">2004</xref>). These studies provide substantial evidence that lipid rafts play an important role in Src/Ras/Raf/ERK/ NF-кB signaling during JEV infection, thereby influencing host immune responses. In addition, Bentley and coworkers (Bentley et al. <xref ref-type="bibr" rid="CR23">2007a</xref>) also demonstrated that rhinovirus (RV) activates PI3K and Akt, which leads to IL-8 expression. Further, they observed that RV colocalizes with Src, PI3K, and Akt in membrane rafts. These and several related findings demonstrate that lipid raft-mediated signaling pathways are regulated during viral infections and play critical role in disease pathogenesis (Bentley et al. <xref ref-type="bibr" rid="CR23">2007a</xref>; Silva et al. <xref ref-type="bibr" rid="CR252">2011</xref>; Ebihara et al. <xref ref-type="bibr" rid="CR65">2008</xref>; Huang et al. <xref ref-type="bibr" rid="CR118">2009b</xref>; Fang et al. <xref ref-type="bibr" rid="CR70">2010</xref>) (Fig. <xref rid="Fig2" ref-type="fig">2</xref>).</p></sec></sec><sec id="Sec5"><title>Lipid rafts and fungal infections</title><p id="Par23">Information regarding the role of lipid rafts in fungal infections is evolving; however, initial studies suggest that rafts facilitate fungal infections by regulating hyphal growth and biofilm formation, and by concentrating virulance factors (VFs) (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>; Farnoud et al. <xref ref-type="bibr" rid="CR74">2015</xref>).</p><sec id="FPar8"><title>Role of the host rafts during fungal infection and modulation of host signaling</title><p id="Par24">The connection of fungal infection with lipid rafts has not been extensively explored; however, evidences for modulation in host cell signaling pathways by mycopathogens has been demonstrated. Paracoccidioidomycosis is one of common fungal disease with high prevalence in South and Central America and is caused by <italic>Paracoccidioides brasiliensis</italic>. Infection with <italic>P. brasiliensis</italic> promotes the aggregation of lipid rafts in epithelial cells, which then support fungal adhesion and activation of Src kinases (Fig. <xref rid="Fig4" ref-type="fig">4</xref>). Localization of Ganglioside (GM1) in the host membrane microdomains allows <italic>P. brasiliensis</italic>-epithelial cell contact and fugal adhesion, which was found to be inhibited by methyl-β-cyclodextrin (MβCD) (Maza et al. <xref ref-type="bibr" rid="CR171">2008</xref>). Moreover, invasion by <italic>Candida albicans</italic> or <italic>P. brasiliensis</italic> leads to the activation of host cell tyrosine kinases which can be regulated by tyrosine kinase inhibitors (Belanger et al. <xref ref-type="bibr" rid="CR22">2002</xref>; Monteiro da Silva et al. <xref ref-type="bibr" rid="CR180">2007</xref>). Further, hyphal growth and biofilm formation facilitate invasive growth of <italic>Cryptococcus neoformans</italic> into the central nervous system; for which the pathogen needs to travel across the blood-brain barrier composed of human brain microvascular endothelial cells (HBMECs). CD44 is the <italic>C. neoformans</italic> receptor believed to be anchored in lipid rafts on the surface of HBMECs during infection. It is known that in <italic>caveolin-1</italic> knockdown HBMECs, GM1 and CD44 protein become randomly distributed and clustered into irregular-islands on the cell surface (Long et al. <xref ref-type="bibr" rid="CR154">2012</xref>). This suggests an important structural role of caveolin-1 in <italic>C. neoformans</italic> invasion. Activated PKCα, can directly interact with caveolin-1, on the plasma membrane, and is required for <italic>C. neoformans</italic> invasion into HBMEC (Jong et al. <xref ref-type="bibr" rid="CR124">2008</xref>; Oka et al. <xref ref-type="bibr" rid="CR198">1997</xref>). Finally, the microsporidiam parasite, <italic>Encephalitozoon cuniculi</italic>, which affects the nervous system, as well as the respiratory and digestive tracts, has been shown to localize to lipid rafts. While residing in a parasitophorous vacuole, this pathogen is surrounded by host cell lipids; which could be labeled with DilC16 (1,1′-dihexadecyl-3,3,3′,3′-tetramethylindocarbocyanine), a marker for lipid rafts, and DiO (3,3′-dilinoleyloxacarbocyanine), a marker for non-raft membrane domains. These results suggest that rafts contribute to the formation of parasitophorous vacuole membrane (Ronnebaumer et al. <xref ref-type="bibr" rid="CR234">2008</xref>) and also that mycopathogens may also infect cells in a raft-dependent manner (Vieira et al. <xref ref-type="bibr" rid="CR290">2010</xref>).<fig id="Fig4"><label>Fig. 4</label><caption><p>Fungal infection in association with lipid rafts and host cell signaling. Fungal infection promotes the aggregation of lipid rafts in epithelial cells. Localization of ganglioside (GM1) in the host membrane microdomains allows cell contact and fugal adhesion. Fungal adhesion leads to activation of PKCα and Src protein tyrosine kinases leading to downstream signaling events in the host cells. Lipid rafts facilitate fungal infections by regulating hyphal growth, biofilm formation, concentrating virulance factors, and drug resistance</p></caption><graphic xlink:href="10565_2017_9386_Fig4_HTML" id="MO4"></graphic></fig></p></sec><sec id="FPar9"><title>Role of fungal rafts in virulence and drug resistance</title><p id="Par25">The primary raft-forming lipids in <italic>C. albicans</italic>, a dimorphic opportunistic pathogen, include ergosterol and glycosphingolipids, while the transporter of N-acetylglucosamine protein (Ngt1), an efflux pump and drug transporter protein (CaCdr1p), GPI-anchored protein (Gas1p), and proton pump protein (Pma 1) are the major proteins associated with these rafts (Martin and Konopka <xref ref-type="bibr" rid="CR169">2004</xref>; Simonetti et al. <xref ref-type="bibr" rid="CR254">1974</xref>; Pasrija et al. <xref ref-type="bibr" rid="CR210">2008</xref>). <italic>C. albicans</italic> rafts are capable of forming biofilms creating a protected niche for microorganism against antibiotics and a source of persistent infection. The efficiency of biofilm formation can be significantly reduced after treatment with myriocin and aureobacidin suggesting an important role of sphingolipids (lipid rafts) in biofilms formation (Martin and Konopka <xref ref-type="bibr" rid="CR169">2004</xref>; Lattif et al. <xref ref-type="bibr" rid="CR143">2011</xref>). Furthermore, displacement of these proteins from membrane by disruption of ergosterol or the sphingolipid biosynthesis pathway negatively influences the drug resistance of fungi and suggests the importance of raft assembly for localization of these proteins (Wang et al. <xref ref-type="bibr" rid="CR293">2012</xref>). Similarly, when CaCdr1p is depleted from DRMs, <italic>Saccharomyces cerevisiae</italic> becomes prone to methotrexate and fluconazole (Pasrija et al. <xref ref-type="bibr" rid="CR210">2008</xref>). Furthermore, ergosterol depletion has also been shown to impair phagocytosis of <italic>Histoplama capsulatum</italic>, which may result from the release of proteins with anti-phagocytic function (Tagliari et al. <xref ref-type="bibr" rid="CR272">2012</xref>). Although, secretion of anti-phagocytic proteins has been demonstrated in case of <italic>C. neoformans</italic>, the direct link with ergosterol depletion and secretion of these proteins during <italic>H. capsulatum</italic> infection has not yet been established (Tagliari et al. <xref ref-type="bibr" rid="CR272">2012</xref>; Luberto et al. <xref ref-type="bibr" rid="CR159">2003</xref>). While studying chitosan-resistant and chitosan-sensitive filamentous fungi, Palma-Guerrero and coworkers demonstrated the importance of fungal rafts in drug resistance. They identified an <italic>Neisseria crassa</italic> desaturase mutant with chitosan resistance and high membrane rigidity. The polymeric compound chitosan exerts its fungicial effect by permeabilizing plasma membrane of filamentous fungi (Palma-Guerrero et al. <xref ref-type="bibr" rid="CR206">2010</xref>). Additionally, the role of detergent-resistant membranes in fungi for concentrating VFs-phospholipase B1 and Cu/Zn superoxide dismutase; and proton pump protein Pma1 was demonstrated by Siafakas et al. and Holyoak groups, respectively (Siafakas et al. <xref ref-type="bibr" rid="CR250">2006</xref>; Holyoak et al. <xref ref-type="bibr" rid="CR115">1996</xref>). Several reports have demonstrated the functional role of these VFs in evading hosts immune responses and Pma1 in the pathogenicity of <italic>C. neoformans</italic> (Farnoud et al. <xref ref-type="bibr" rid="CR73">2014</xref>).</p></sec></sec><sec id="Sec6"><title>Perspectives</title><p id="Par26">There is abundance of literature defining the role of lipid rafts in several pathological conditions including Alzheimer’s disease, Prion disease (Campbell et al. <xref ref-type="bibr" rid="CR39">2001</xref>; Peters et al. <xref ref-type="bibr" rid="CR216">2003</xref>; Liao et al. <xref ref-type="bibr" rid="CR149">2001a</xref>; Nguyen and Taub <xref ref-type="bibr" rid="CR190">2002a</xref>; Liao et al. <xref ref-type="bibr" rid="CR151">2003</xref>), abnormalities associated with the cardiovascular system such as hypertension and cardiac hypertrophy (Fantini et al. <xref ref-type="bibr" rid="CR71">2002</xref>; Peters et al. <xref ref-type="bibr" rid="CR216">2003</xref>; Liao et al. <xref ref-type="bibr" rid="CR149">2001a</xref>; Golde and Eckman <xref ref-type="bibr" rid="CR89">2001</xref>) and during bacterial and viral infections. Therefore, understanding the regulation and formation/composition of rafts is imperative for the design of therapeutic strategies for prevention and cure of related pathologies, as well as to aid in patient management. For example, the use of statins in cancer chemotherapy has been suggested as these drugs have been shown to alter endothelial cell function and inflammatory responses (Mo and Elson <xref ref-type="bibr" rid="CR179">2004</xref>). However, the effect of statins is not directly mediated through cholesterol, but is rather through their effect on isoprenoids, which share initial biochemical synthetic steps with cholesterol and play important roles in anchoring several GTPases in the membrane (Vaughan <xref ref-type="bibr" rid="CR288">2003</xref>). Similar effects including the activation of GTPase were reported in cholesterol depletion and repletion models used to study the raft function in cell culture models (Pierini et al. <xref ref-type="bibr" rid="CR217">2003</xref>; Nagao et al. <xref ref-type="bibr" rid="CR183">2007</xref>). In this regard, a membrane-tethering inhibitor of β-secretase that targets endosomes was designed for treatment of Alzheimer’s disease (Rajendran et al. <xref ref-type="bibr" rid="CR228">2008</xref>). This same idea may be employed for development of small lipophilic inhibitors to target raft-anchored proteins that are activated in membrane compartments.</p><p id="Par27">Earlier reports have also demonstrated that modulating the structure/composition of rafts can lead to inhibition of the infection cycle of HIV-1, which enters the host cell through rafts, and can regulate raft-mediated signaling pathways. SP01A, a widely used inhibitor of HIV-1 infection, affects cholesterol synthesis and regulates the cholesterol content of rafts thereby preventing HIV-1 fusion with CD4+ cells. Likewise, the use of anti-raft drugs shows clear promise as an alternative to antibiotics to help reduce the threat of drug-resistant bacteria. Further, targeting lipid raft formation in bacteria using small molecules has also been shown to reduce their virulence by regulating diverse processes including exoprotease production, biofilm formation, and attachment (Kong et al. <xref ref-type="bibr" rid="CR128">2006</xref>; Liu et al. <xref ref-type="bibr" rid="CR153">2008</xref>). However, careful assessment of the strategies utilized should be made while targeting cholesterol in the rodent models, as there exists quantitative and qualitative difference in its balance as compared to humans. Further, high concentrations of cholesterol at several anatomical sites would also impair the ability to uniformly target cholesterol for pathological conditions that effect various tissues/organs (Dietschy and Turley <xref ref-type="bibr" rid="CR58">2002</xref>).</p><p id="Par28">Given that there is a unique assembly of proteins and lipids during the formation of signaling/raft domains in response to infection with various pathogens, alteration of the composition of lipid rafts through nutritional intervention may be other interesting approach to combat pathogens and modulate the inflammatory responses. This strategy has received wide acceptance in the recent years and growing evidence suggests that consumption of n-3 long-chain polyunsaturated fatty acids (LCPUFAs) can reduce the risk of cardiovascular disease and breast cancer. In this context, n-3 LCPUFA has been shown to alter the partitioning of proteins and composition of rafts including the reduction of cholesterol (Hashimoto et al. <xref ref-type="bibr" rid="CR109">1999</xref>) and caveolae (Ma et al. <xref ref-type="bibr" rid="CR162">2004</xref>), and has been shown to regulate Akt and NF-кB activation(Schley et al. <xref ref-type="bibr" rid="CR243">2007</xref>). In addition, n-3 LCPUFA induces p38MAPK and EGFR phosphorylation, which leads to increased apoptosis in tumor cells (Schley et al. <xref ref-type="bibr" rid="CR243">2007</xref>; Tikhomirov and Carpenter <xref ref-type="bibr" rid="CR277">2004</xref>). An extensive report was published by Turk and Chapkin (Turk and Chapkin <xref ref-type="bibr" rid="CR283">2013</xref>) describing the regulation of lipid raft size, composition, and associated signaling mechanisms by n-3 LCPUFA. These findings underscore the need to further assess the therapeutic potential of n-3 LCPUFA in disease states mediated by lipid raft-associated processes.</p></sec><sec id="Sec7"><title>Conclusions</title><p id="Par29">With the majority of the scientific community focusing on DNA, RNA, and proteins to understand the pathogenesis of disease, the role of lipids has remained relatively unexplored. However, recent advances in the field of membrane microdomains/lipid rafts research has opened new avenues to investigate alternative therapeutic intervention strategies for many diseases. Although there is abundant literature suggesting important role of lipid rafts in bacterial, viral, and fungal infections, several questions still remain to be answered in order to define and target raft-mediated responses. Thus, impairment of bacterial and viral entry and propagation in the host in response to deviations/alterations in functional membrane microdomains warrants further study in order to better assess their role in bacterial and viral infections. Further, the involvement of structural components in terms of regulating rafts size, the concentration of lipids in microdomains, the specificity of protein and lipid clustering, and rafts scaffolding during disease pathogenesis are areas requiring additional focus and potentially, even more sophisticated techniques. Addressing these particular aspects of functional membrane microdomains will lead to a better understanding of disease mechanisms and potentially more effective treatment strategies including cell-based or personalized medicine approaches. The former approach is based on the concept of delivering therapeutic agents/drugs to specific cell types using nano-particle based delivery of drugs to the plasma membrane of cells for raft-dependent intracellular trafficking (Partlow et al. <xref ref-type="bibr" rid="CR208">2008</xref>). With regard to personalized medicine approaches, lipidomics monitoring can provide a description of the concentration, structure, and function of complete sets of lipids as well as information regarding the interaction of lipids with proteins and other metabolites. This information can be utilized to design a personalized strategy to restore membrane balance using lipids and cofactors from nutritional sources (Escriba <xref ref-type="bibr" rid="CR68">2006</xref>). In addition, recent reports have suggested increased individual disease susceptibility to several diseases due to the limitations of several therapeutic proteins like growth factors and antibodies to reach the cytoplasm of diseased cells. These limitations can be overcome through covalent modification with glycolipid structures (GPI anchors) resulting in directed lipid raft-mediated signaling. Furthermore, research and clinical studies using anticancer drugs that target lipid messengers or their carriers are ongoing. These drugs are designed to disrupt crosstalk between cells within the tumor microenvironment and cancer cells (Muller <xref ref-type="bibr" rid="CR181">2011</xref>). Future studies aiming to reduce the generation and secretion of exosomes, which possess the bioactive lipids found in the extracellular space in tumor environment, have also been proposed by the experts in cancer research. These new approaches hold promise and the potential to offer novel therapeutic targets with translation potential for future intervention studies.</p></sec></body><back><fn-group><fn><p>Prathyusha Bagam and Dhirendra P. Singh contributed equally.</p></fn></fn-group><ack><title>Acknowledgements</title><p>This work was supported by Young Clinical Scientist Award from the Flight Attendant Medical Research Institute (FAMRI-123253_YCSA_Faculty), NIH R15 (7 R15 ES023151 02), Southern University Foundation Grant (FY2017-017), and LBRN Startup Grant (2P20GM103424-14-Subaward No. 100011) to SB.</p></ack><notes notes-type="ethics"><title>Compliance with ethical standards</title><notes notes-type="COI-statement"><title>Conflict of interest</title><p id="Par30">The authors declare that they have no conflict of interest.</p></notes></notes><ref-list id="Bib1"><title>References</title><ref id="CR1"><element-citation publication-type="journal"><person-group 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